publications

Watanabe lab

Preprints

  1. Eddings, C. and Watanabe, S., (2025) Ultrafast endocytosis in mouse cortical inhibitory synapses,  BioRxiv, DOI: 10.1101/2025.06.06.658279  BioRxiv
  2. Ma, S., Watanabe, S. *, Gillespie, D.C. *, (2024) Ultrastructure of immature synaptic inputs in the lateral superior olive of the rodent brainstem,  BioRxiv, DOI: 10.1101/2024.08.09.606139. *correspondence BioRxiv
  3. Imoto, Y., Ma, Y., Itoh, K., Blumrich, E., Matsubayashi, H., Liu, J., Wu, B., Cousin, M.A., Ha, T., Inoue, T., Watanabe, S., (2022) Dynamin forms liquid-like condensates at synapses to support ultrafast endocytosis, DOI: 10.1101/2022.06.01.494432. link

Peer-reviewed

  1. Eddings, C., Fan, M., Imoto, Y., Itoh, K., McDonald, X., Eilers, J., Anderson, W.S., Worley, P.F., Lippmann, K., Nauen, D.W., Watanabe, S., (2026) Ultrastructural membrane dynamics of mouse and human cortical synapses, Neuron, DOI: 10.1016/j.neuron.2025.10.030 link pdf BioRxiv Hopkins News
  2. Watanabe, S., (2025), Synaptic vesicle recycling through the lens of ultrafast endocytosis, Annual Review of Neuroscience, 48:297-310, DOI: 10.1146/annurev-neuro-112723-040652  link  pdf
  3. Ogunmowo, T., Hoffmann, C., Pepper, R., Wang, H., Gowrisankaran, S., Ho, A., Raychaudhuri, S., Cooper, B.H., Milosevic, I., Milovanovic, D., Watanabe, S., (2025) Intersectin and Endophilin condensates prime synaptic vesicles for release site replenishment, Nature Neuroscience, DOI: 10.1038/s41593-025-02002-4. link pdf BioRxiv Hopkins News
  4. Imoto, Y. and Watanabe, S. (2025) Beyond clathrin: decoding the mechanism of ultrafast endocytosis, Journal of Physiology, DOI: 10.1152/physiol.00041.2024   link pdf
  5. Griswold, J.M., Bonilla-Quintana, M., Pepper, R., Lee, C.T., Raychaudhuri, S., Ma, S., Gan, Q., Syed, S., Zhu, C., Bell, M., Suga, M., Yamaguchi, Y., Chéreau, R., Nägerl, U.V., Knott, G., Rangamani, P.*, Watanabe, S.*, (2024) Membrane mechanics dictate axonal pearls-on-a-string morphology and function, Nature Neuroscience, DOI: 10.1038/s41593-024-01813-1. link BioRxiv Science cover story  ScienceNews Hopkins News MBL News
  6. Wang, H., Vant, J., Zhang, A., Sanchez, R., Wu, Y., Micou, M.L., Luczak, V., Whiddon, Z., Carlson, N., Yu, S.B., Jabbo, M., Yoon, S., Abushawish, A.A., Ghassemian, M., Masubuchi, T., Gan., Q., Watanabe, S., Giffis, E., Hammarlund, M., Singharoy, A., Pekkurnaz, G., (2024) Organization of a functional glycolytic metabolon on mitochondria for metabolic efficiency, Nature Metabolism, DOI: 10.1038/s42255-024-01121-9 link pdf cover story
  7. Imoto, Y., Xue, J., Luo, L., Raychaudhuri, S., Itoh, K., Ogunmowo, T., Ho, A., Ma, Y., Craft, G.E., Kwan, A.H., Mackay, J.P., Ha, T., Watanabe, S.*, and Robinson, P.J.*, (2024) Dynamin 1xA interacts with Endophilin A1 via its spliced long C-terminus for ultrafast endocytosis, EMBO J., DOI: s44318-024-00145-x. link pdf BioRxiv cover story *correspondence.
  8. Dong, Y., Johnson, B.A., Ruan, L., Zineldin, M., Liu, A.Z., Raychaudhuri, S., Chiu, I., Zhu, J., Smith, B., Zhao, N., Searson, P., Watanabe, S., Donowitz, M., Larman, T.C., Li, R., Disruption of epithelium integrity by inflammation-associated fibroblasts through prostaglandin signaling, (2024) Science Advances, 10:14, DOI: 10.1126/sciadv.adj7666 link pdf
  9. Wu, Z., Kusick, G.F., Raychaudhuri, S., Itoh, K., Chapman, E.R.*, Watanabe, S.*, (2024) Synaptotagmin 7 supplies docked vesicles for Doc2ɑ-triggered asynchronous neurotransmitter release, eLife, 12:RP90632, DOI: 10.7554/eLife.90632 link pdf BioRxiV
  10. Wu Y., Ding, C., Behrang, S., Weinreb, A., Swaim, G., Hao, H., Yogev, S., Watanabe, S., Hammarlund, M., (2024) Polarized localization of kinesin-1 and RIC-7 drives axonal mitochondria anterograde transport, Journal of Cell Biology, 223 (5): e202305105. DOI:10.1083/jcb.202305105. link pdf
  11. Nakamura, H., Rho, E., Lee, C.T., Itoh, K., Deng, D., Watanabe, S., Razavi, S., Matsubayashi, H.T., Zhu, C., Jung, E., Rangamani, P., Watanabe, S., Inoue, T., (2023) ActuAtor, a Listeria-inspired molecular tool for generating force in living cells: Controlled deformation of intracellular organizations, Cell Reports, 113089 DOI: 10.1016/j.celrep.2023.113089 link pdf
  12. Ogunmowo, T.H., Jing, H., Raychaudhuri, S.,  Kusick, G.F., Imoto, Y., Li, S., Itoh, K., Ma, Y.,  Jafri, H., Dalva, M.B., Chapman, E.R., Ha, T.,  Watanabe, S.*, Liu, J.*, (2023), Membrane compression by exocytosis triggers ultrafast endocytosis, Nature Comm. 14:2888. DOI: 10.1038/s41467-023-38595-2 link pdf BioRxiV
  13. Mueller, B.D., Merrill, S.A., Watanabe, S., Liu, P., Singh A., Cherry, A., Silva, M., Wang, Z., Jorgensen, E., (2023), CaV1 and CaV2 calcium channels mediate the release of distinct pools of synaptic vesicles. eLife. link pdf BioRxiv
    12:e81407. doi: 10.7554/eLife.81407  link  pdf BioRxiV
  14. Vettkotter, D., Schneider, M., Goulden, B.D., Dill, H., Liewald, J., Zeiler, S., Guldan, J., Arda Ates, Y., Watanabe, S., Gottschalk, A., (2022) Rapid and reversible optogenetic silencing of synaptic transmission by clustering of synaptic vesicles. Nature Comm. DOI: 10.1038/s41467-022-35324-z link pdf BioRxiV 
  15. Watanabe, S., Nihongaki, Y., Itoh, K., Watanabe, S., Inoue, T., (2022), Defunctionalizing intracellular organelles such as mitochondria and peroxisomes with engineered phospholipase A/acyltransferases. Nature Comm. 29;13(1):4413 DOI: 10.1038/s41467-022-31946-5 link pdf BioRxiV
  16. Kusick, G., Ogunmowo, T., Watanabe, S., (2022) Transient docking of synaptic vesicles: implications and mechanisms. Current Opinion in Neurobiology. 74:102535. link pdf
  17. Imoto, Y., Raychaudhuri, S.*, Ma, Y.*, Fenske, P., Sandoval, E., Itoh, K., Blumrich, E., Matsubayashi, H.T.,  Mamer, L., Zarebidaki, F., Söhl-Kielczynski, B., Trimbuch, T., Nayak, Shraddha, Iwasa, J., Liu, J., Wu, B., Ha, T., Inoue, T., Jorgensen, E.M., Cousin, M., Rosenmund, C., Watanabe, S., (2022), Dynamin is primed at endocytic sites for ultrafast endocytosis, Neuron, S0896-6273(22)00548-7. link pdf BioRxiV featured by nature reviews
  18. Birdsall, V., Kirwan K., Zhu, M., Imoto, Y., Wilson, S.M., Watanabe, S., and Waites, C.,  (2022) Axonal transport of Hrs is activity dependent and facilitates synaptic vesicle protein degradation. Life Science Alliance, 5 (10):e202000745. link pdf BioRxiV
  19. Vevea, J.D., Kusick, G.F., Courtney, K.C., Chen, E., Watanabe, S., and Chapman, E., Synaptotagmin 7 is targeted to the axonal plasma membrane through γ-secretase processing to promote synaptic vesicle docking in mouse hippocampal neurons, (2021) eLife, 10:e67261, DOI: 10.7554/eLife.67261. link pdf BioRxiv
  20. Li, S., Raychaudhuri, S., Lee, S.A., Wang, J., Kusick, G.F., Prater, C., Syed, S., Falahati, H., Ramos, R., Bartol, T.M., Hosy, E., and Watanabe., S., (2021) Asynchronous release sites are aligned with NMDA receptors at mouse hippocampal synapses. Nature Communications. DOI: 10.1038/s41467-021-21004-x. link pdf BioRxiV
  21. Watanabe, S., Davis, M.W., Kusick, G., Jorgensen, E.M., (2020) SynapsEM: computer-assisted synapse morphometry, Frontiers in Synaptic Neuroscience, DOI: 10.3389/fnsyn.2020.584549 link pdf BioRxiV
  22. Kusick, G. F. Chin, M., Lippmann, K., Adula, K.P., Davis, M.W., Jorgensen, E.M., and Watanabe, S. (2020) Synaptic vesicles transiently dock to refill release sites. Nature Neuroscience, 23,  1329–1338, DOI: 10.1038/s41593-020-00716-1  link pdf BioRxiV
  23. Ogunmowo, T., Raychaudhuri, S., Kusick, G., Li, S., and Watanabe, S., (2020) Correlative Super Resolution and Electron Microscopy to Detect Molecules in Their Native Cellular Context, Volume Microscopy, 155, 1-13 link pdf
  24. Itoh, K., Murata, D., Kato, T., Yamada, T., Araki, Y., Saito, A., Adachi, Y., Igarashi, A., Li, S., Pletnikov, M., Huganir, R.L., Watanabe, S., Kamiya, A., Iijima, M., and Sesaki, H. (2019) Brain-specific Drp1 regulates postsynaptic endocytosis and dendrite formation independently of mitochondrial division. eLife DOI: 10.7554/eLife.44739. link pdf
  25. Gan, Q., and Watanabe, S., (2018), Synaptic vesicle endocytosis in different model systems. Frontiers in Cellular Neuroscience, doi:10.3389/fncel.2018.00171. link  pdf
  26. Watanabe, S., Mamer, L.E., Raychaudhuri, S., Luvsanjav, D., Eisen, J., Trimbuch, T., Söhl-Kielczynski, B., Fenske, P., Milosevic, I., Rosenmund, C., and Jorgensen, E.M. (2018). Synaptojanin and endophilin mediate neck formation during ultrafast endocytosis. Neuron. 98(6), 1184-1197. link pdf
  27. Nakamura, H, Lee, A, Afshar, A, Watanabe, S., Rho, E, Razavi, S, Suarez, A Lin, Y., Tanigawa, M., Huang, B., DeRose, R., Bobb, D., Hong, W., Gabelli, S.B., Goutsias, J., Inoue, T.  (2018). Intracellular Production of Hydrogels and Synthetic RNA Granules by Multivalent Interactions. Nature Materials, 2018; 17, 79–89. link pdf
  28. Chanaday, N. R., Cousin, M., Milosevic, I., Watanabe, S.*, and Morgan, J. *, The synaptic vesicle cycle revisited: New insights into the modes and mechanisms, Journal of Neuroscience, 2019; 39(42):8209-8216 *corresponding authors link pdf
  29. Topalidou I, Chen PA, Cooper K, Watanabe S, Jorgensen EM, Ailion M, (2017) The NCA-1 and NCA-2 Ion Channels Function Downstream of Gq and Rho To Regulate Locomotion in Caenorhabditis elegans. Genetics, 2017; doi: 10.1534/genetics.116.198820 link pdf
  30. Li S, Raychaudhuri S, Watanabe S, (2017), Flash-and-freeze: A novel technique to capture membrane dynamics by electron microscopy, JoVE, 2017;123. doi: 10.3791/55664 link pdf
  31. Watanabe S. and Boucrot E. Fast and ultrafast endocytosis, Curr Opin Cell Biol. 2017;5;47:64-71. link pdf
  32. Watanabe S, Flash-and-freeze: coordinating optogenetic stimulation with rapid freezing to visualize membrane dynamics at synapses with millisecond resolution, Frontiers in Synaptic Neuroscience, 2016:8,24  link  pdf

Watanabe other publications

  1. Watanabe S.  Slow or fast? A tale of synaptic vesicle recycling, Science 2015;350: 46-7. link pdf
  2. Watanabe S, Trimbuch T, Camacho-Perez M, Rost BR, Brokowski B, Söhl-Kielczynski B, Felies A, Rosenmund C, Jorgensen EM. Clathrin regenerates synaptic vesicles from endosomes, Nature 2014;515: 228-233. link pdf
  3. Ailion M, Hannemann M, Dalton S, Pappas A, Watanabe S, Hegermann J, Liu Q, Han HF, Gu M, Goulding MQ, Sasidharan N, Schuske K, Hullett P, Eimer S, Jorgensen EM, Two rab2 interactors regulate dense-core vesicle maturation, Neuron 2014;82: 167-180. link pdf
  4. Watanabe S, Rost BR, Camacho-Perez M, Davis MW, Söhl-Kielczynski B, Rosenmund C, Jorgesen EM. Ultrafast endocytosis at mouse hippocampal synapses, Nature 2013:504; 242-247.   link pdf
  5. Watanabe S, Liu Q, Davis MW, Hollopeter G, Thomas N, Jorgensen NB, Jorgensen EM. Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions, Elife 2013;2: e00723. link pdf
  6. Shao Z, Watanabe S, Christensen R, Jorgensen EM, Colón-Ramos DA, Synapse location during growth depends on glia location, Cell 2013;154: 337-350. link pdf
  7. Jurrus E, Watanabe S, Giuly RJ, Paiva ARC, Ellisman M, Jorgensen EM, Tasdizen T. Semi-automated Neuron Boundary Detection and Nonbranching Process Segmentation in Electron Microscopy Images, Neuroinformatics. 2013;1: 5-29 link pdf
  8. Gu M, Liu Q, Watanabe S, Sun L, Hollopeter G, Grant B, Jorgensen EM. AP2 subunits contribute independently to synaptic vesicle endocytosis, Elife, 2013;5:e00190. link pdf
  9. Watanabe S, Richards J, Hollopeter G, Hobson RJ, Davis MW, Jorgensen EM. nano-fEM: protein localization using photo-activated localization microscopy and electron microscopy, JoVE 2012;70: e3995. link  pdf
  10. Mullen GP, Grundahl KM, Gu M, Watanabe S, Hobson RJ, Crowell JA, McManus JR, Matthews EA, Jorgensen EM, Rand JB. UNC-41/stonin functions with AP2 to recycle synaptic vesicles in Caenorhabditis elegans, PLoS One 2012;7: e40095. link pdf
  11. Ernstrom GG, Weimer R, Pawar DRL, Watanabe S, Hobson RJ, Greenstein D, Jorgensen EM. V-ATPase V1 sector is required for corpse clearance and neurotransmission in C. elegans, Genetics 2012;191: 461-475. link pdf
  12. Oikonomou G, Perens EA, Lu Y, Watanabe S, Jorgensen EM, Shaham S. Opposing activities of LIT-1/NLK and DAF-6/patched-related direct sensory compartment morphogenesis in C. elegans. PLoS Biol. 2011;9: e1001121. link pdf
  13. Park M, Watanabe S, Poon VYN, Ou CY, Jorgensen EM, Shen K. CYY-1/cyclin Y and CDK-5 differentially regulate synapse elimination and formation for rewiring neural circuits. Neuron 2011;70: 742–757. link pdf
  14. Hobson RJ, Liu Q, Watanabe S, Jorgensen EM. Complexin maintains vesicles in the primed state in C. elegans. Curr. Biol. 2011;21: 106–113. link pdf
  15. Watanabe S, Punge A, Hollopeter G, Willig KI, Hobson RJ, Davis MW, Hell SW, Jorgensen EM. Protein localization in electron micrographs using fluorescence nanoscopy. Nat. Methods 2011;8: 80–84. link pdf
  16. Jurrus E, Paiva ARC, Watanabe S, Anderson JR, Jones BW, Whitaker RT, Jorgensen EM, Marc RE, Tasdizen T. Detection of neuron membranes in electron microscopy images using a serial neural network architecture. Med Image Anal 2010;14: 770–783. link pdf
  17. Ou, CY, Poon VY, Maeder CI, Watanabe S, Lehrman EK, Fu AKY, Park M, Fu WY, Jorgensen EM, Ip NY, Shen K. Two cyclin-dependent kinase pathways are essential for polarized trafficking of presynaptic components. Cell 2010:141; 846–858. link pdf
  18. Pellettieri J, Fitzgerald P, Watanabe S, Mancuso J, Green DR, Sánchez-Alvarado A. Cell death and tissue remodeling in planarian regeneration. Dev. Biol. 2010;338: 76–85. link pdf
  19. Sato K, Ernstrom GG, Watanabe S, Weimer RM, Chen CH, Sato M, Siddiqui A, Jorgensen EM, Grant BD. Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools. Proc. Natl. Acad. Sci. U.S.A. 2009;106: 1139–1144. link pdf
  20. Gu M, Schuske K, Watanabe S, Liu Q, Baum P, Garriga G, Jorgensen EM. Mu2 adaptin facilitates but is not essential for synaptic vesicle recycling in Caenorhabditis elegans. J. Cell Biol. 2008;183: 881–892. link pdf
  21. Hammarlund M, Watanabe S, Schuske K, Jorgensen EM. CAPS and syntaxin dock dense core vesicles to the plasma membrane in neurons. J. Cell Biol. 2008;180: 483–491. link pdf
  22. Jospin M, Watanabe S, Joshi D, Young S, Hamming K, Thacker C, Snutch TP, Jorgensen EM, Schuske K. UNC-80 and the NCA ion channels contribute to endocytosis defects in synaptojanin mutants. Curr. Biol. 2007;17: 1595–1600. link pdf
  23. Hammarlund M, Palfreyman MT, Watanabe S, Olsen S, Jorgensen EM. Open syntaxin docks synaptic vesicles. PLoS Biol. 2007;5: e198. Co-first author. link pdf
  24. Schuske K, Palfreyman MT, Watanabe S, Jorgensen EM. UNC-46 is required for trafficking of the vesicular GABA transporter. Nat. Neurosci. 2007;10: 846–853. link pdf